Application of microencapsulated Trichoderma spp. against Moniliophthora roreri during the vegetative development of cocoa

Daniel  Avilés; Fernando  Espinoza; Liliana  Villao; José  Alvarez; Daynet  Sosa; Efrén  Santos-Ordóñez; Luis  Galarza

doi:10.17268/sci.agropecu.2023.045

Authors

Daniel Avilés Centro de Investigaciones Biotecnológicas del Ecuador, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0001-7829-3075
Fernando Espinoza Centro de Investigaciones Biotecnológicas del Ecuador, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0002-2051-2682
Liliana Villao Centro de Investigaciones Biotecnológicas del Ecuador, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0002-2677-1415
José Alvarez Universidad San Francisco de Quito (USFQ), Quito, Ecuador. https://orcid.org/0000-0002-4019-4319
Daynet Sosa Facultad de Ciencias de la Vida, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0001-5403-9072
Efrén Santos-Ordóñez Facultad de Ciencias de la Vida, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0002-0749-6024
Luis Galarza Centro de Investigaciones Biotecnológicas del Ecuador, Campus Gustavo Galindo, ESPOL Polytechnic University, Escuela Superior Politécnica del Litoral, ESPOL, Guayaquil, Ecuador. https://orcid.org/0000-0002-2870-4080

DOI:

https://doi.org/10.17268/sci.agropecu.2023.045

Keywords:

Microencapsulation, biocontrol, Trichoderma, bioproducts, Moniliophthora roreri, Theobroma cacao

Abstract

Ecuador is one of the leading producers of fine aroma cocoa worldwide, involving around 100,000 producer families. On the American continent, the largest producer is Brazil, with 18%, followed by Ecuador and Colombia, and it is estimated that more than 20 million people depend directly on this crop. Moniliophthora roreri, the causal agent of frost pot rot, has been a cause of great concern due to the production losses it has caused, which in 2022 amounted to 80% in different cocoa-producing provinces of Ecuador and worldwide losses of 30% performance they are estimates. This study aimed to determine the biological control potential of microcapsules made with Trichoderma spp spore solution against M. roreri. The In vitro evaluation of the microcapsules did not show significant results in the percentage of inhibition, and this was not the case in the direct evaluation on the farm, where the severity in the 15-day-old fruits showed 0% external and internal affectation with the use of microcapsules in its liquid presentation. Additionally, the evolution of the microcapsules in 28-day-old fruits was observed in severity from 1 to 25% with intercalated applications. Beneficial fungi were applied first, followed by pathogens; though, when the pathogen was applied first, and then the beneficial fungus, the increased severity of external and internal disease was 26-75% and 80-100%, respectively. In conclusion, using microcapsules based on Trichoderma strains at the early ages of the fruits generates protection against M. roreri throughout the vegetative development of the fruit.

References

Bailey, B. A., Ali, S. S., Strem, M. D., & Meinhardt, L. W. (2018). Morphological variants of Moniliophthora roreri on artificial media and the biotroph/necrotroph shift. Fungal Biol. https://doi.org/10.1016/j.funbio.2018.03.003

Bailey, B. A., & Meinhardt, L. W. (2016) Cacao diseases: A history of old enemies and new encounters. Publisher Springer Cham. 633 pp. https://doi.org/10.1007/978-3-319-24789-2

Carrera, L. (2017). Encapsulación de Trichoderma asperellum en partículas biopoliméricas con quitosanos de diferentes pesos moleculares para el control biológico de Moniliophthora roreri. Tesis bachiller, Universidad San Francisco de Quito. Ecuador.

Chun, H., Kim, C. H., Cho, Y. H. (2014). Microencapsulation of Lactobacillus plantarum DKL 109 using external ionic gelation method. Korean J Food Sci Anim Resour, 34(5), 692-699. https://doi.org/10.5851/kosfa.2014.34.5.692

Cuello, R. E. G., Mendoza, J. P., & Alcázar, L. B. M. (2015). Efecto de la microencapsulación sobre la viabilidad de Lactobacillus delbrueckii sometido a jugos gástricos simulados. Información Tecnológica, 26(5), 11-16. https://doi.org/10.4067/S0718-07642015000500003

Ezziyyani, M., Pérez Sánchez, C., Requena, M., et al. (2004). Biocontrol por Streptomyces rochei-Ziyani-, de la podredumbre del pimiento (Capsicum annuum L.) causada por Phytophthora capsici. An Biol, 26, 69–78.

Fernández, R., & Suárez, C. (2009). Antagonismo in vitro de Trichoderma harzianum Rifai sobre Fusarium oxysporum Schlecht f sp passiflorae en maracuyá (Passiflora edulis Sims var. Flavicarpa) del municipio zona bananera colombiana. Rev. Fac. Nal. Agr. Medellín, 62(1), 4743-4748.

Fernández-Sandoval, M. T., Ortiz-García, M., Galindo, E., & Serrano-Carreón, L. (2012). Cellular damage during drying and storage of Trichoderma harzianum spores. Process Biochemistry, 47, 186–194. https://doi.org/10.1016/j.procbio.2011.10.006

Galarza, L., Akagi, Y., Takao, K., et al. (2015). Characterization of Trichoderma species isolated in Ecuador and their antagonistic activities against phytopathogenic fungi from Ecuador and Japan. Journal of General Plant Pathology, 81, 201–210. https://doi.org/10.1007/s10327-015-0587-x

Jaimes, Y., & Aranzazu, F. (2010). Manejo de las enfermedades del cacao (Theobroma cacao L) en Colombia, con énfasis en monilia (Moniliophthora roreri). Colombia. Corpoica. 2010. 90 pp.

Krauss, U., Hidalgo, E., Bateman, R., et al. (2010). Improving the formulation and timing of application of endophytic biocontrol and chemical agents against frosty pod rot (Moniliophthora roreri) in cocoa (Theobroma cacao). Biological Control, 54, 230–240. https://doi.org/10.1016/j.biocontrol.2010.05.011

Leiva, S., Oliva, M., Hernández, E., et al. (2020). Assessment of the potential of Trichoderma spp. strains native to Bagua (Amazonas, Peru) in the biocontrol of frosty pod rot (Moniliophthora roreri). Agronomy, 10(9), 1376. https://doi.org/10.3390/agronomy10091376

Leiva, S., Rubio, K., Díaz-Valderrama, J. R., et al. (2022). Phylogenetic Affinity in the Potential Antagonism of Trichoderma spp. against Moniliophthora roreri. Agronomy, 12(9), 2052. https://doi.org/10.3390/agronomy12092052

Locatelli, G. O., dos Santos, G. F., Botelho, P. S., et al. (2018). Development of Trichoderma sp. formulations in encapsulated granules (CG) and evaluation of conidia shelf-life. Biological Control, 117, 21–29. https://doi.org/10.1016/j.biocontrol.2017.08.020

Loguercio, L. L., Santos, L. S., Niella, G. R., et al. (2009) Canopy-microclimate effects on the antagonism between Trichoderma stromaticum and Moniliophthora perniciosa in shaded cacao. Plant Pathol, 58(6), 1104-1115. https://doi.org/10.1111/j.1365-3059.2009.02152.x

Lopes, A. R. de O., Locatelli, G. O., Barbosa, R. de M., et al. (2020). Preparation, characterization and cell viability of encapsulated Trichoderma asperellum in alginate beads. J Microencapsul, 37, 270–282. https://doi.org/10.1080/02652048.2020.1729884

Mancera-López, M. E., Izquierdo-Estévez, W. F., Escalante-Sánchez, A., et al. (2019). Encapsulation of Trichoderma harzianum conidia as a method of conidia preservation at room temperature and propagation in submerged culture. Biocontrol Sci Technol, 29, 107–130. https://doi.org/10.1080/09583157.2018.1535053

Martinez, Y., Ribera, J., Schwarze, F. W. M. R., & De France, K. (2023). Biotechnological development of Trichoderma - based formulations for biological control. Appl Microbiol Biotechnol, 107(18), 5595-5612. https://doi.org/10.1007/s00253-023-12687-x

Maruyama, C. R., Bilesky-José, N., de Lima, R., & Fraceto, L. F. (2020). Encapsulation of Trichoderma harzianum Preserves Enzymatic Activity and Enhances the Potential for Biological Control. Front Bioeng Biotechnol, 8, 225. https://doi.org/10.3389/fbioe.2020.00225

Mbarga, J. B., Begoude, B. A. D., Ambang, Z., et al. (2014). A new oil-based formulation of Trichoderma asperellum for the biological control of cacao black pod disease caused by Phytophthora megakarya. Biological Control, 77, 15–22. https://doi.org/10.1016/j.biocontrol.2014.06.004

Mejía, B. F., & Alvarado, R. Y. (2016). Evaluación in vitro de hongos nativos antagonistas de Moniliophthora rereri (Cif. & Par., Evans et al.,) en el cultivo de cacao (Theobroma cacao L.). Ingeniería tesis, Universidad Nacional Agraria. Nicaragua.

Mejía, L. C., Rojas, E. I., Maynard, Z., et al. (2008). Endophytic fungi as biocontrol agents of Theobroma cacao pathogens. Biological Control, 46(1), 4-14. https://doi.org/10.1016/j.biocontrol.2008.01.012

Phillips-Mora, W., & Wilkinson, M. J. (2007). Frosty pod of cacao: A disease with a limited geographic range but unlimited potential for damage. Phytopathology, 97(12), 1644-1647. https://doi.org/10.1094/PHYTO-97-12-1644

Qi, Q., Fan, C., Wu, H., et al. (2023). Preparation of Trichoderma asperellum Microcapsules and Biocontrol of Cucumber Powdery Mildew. Microbiol Spectr, 11(3), e05084-22. https://doi.org/10.1128/spectrum.05084-22

Rojas-Sánchez, B., Guzmán-Guzmán, P., Morales-Cedeño, L. R., et al. (2022). Bioencapsulation of Microbial Inoculants: Mechanisms, Formulation Types and Application Techniques. Applied Biosciences, 1(2), 198-220. https://doi.org/10.3390/applbiosci1020013

Serrano, L., Moreno, A. S., Sosa, D., et al. (2021). Biosurfactants synthesized by endophytic Bacillus strains as control of Moniliophthora perniciosa and Moniliophthora roreri. Sci Agric,78(Suppl.), e20200172: https://doi.org/10.1590/1678-992X-2020-0172

Sriwati, R., Chamzurn, T., Soesanto, L., & Munazhirah, M. (2019). Field Application of Trichoderma Suspension to Control Cacao Pod Rot (Phytophthora palmivora). AGRIVITA, Journal of Agricultural Science, 41, 175–182. https://doi.org/10.17503/agrivita.v41i1.2146

Suárez Meza, C. L., Fernández Barbosa, R. J., Valero, N. O., et al. (2008). Antagonismo in vitro de Trichoderma harzianum Rifai sobre Fusarium solani (Mart.) Sacc., asociado a la marchitez en maracuyá. Rev Colomb Biotecnol, 10, 35–43.

Toledo-Hernández, M., Tscharntke, T., Tjoa, A., et al. (2020). Hand pollination, not pesticides or fertilizers, increases cocoa yields and farmer income. Agric Ecosyst Environ, 304, 107160. https://doi.org/10.1016/j.agee.2020.107160